High specificity meets genomic flexibility in the Siphamia-Photobacterium symbiosis

Abstract

Host-microbe symbioses must balance partner specificity with enough flexibility to remain adaptable to environmental change. The Siphamia-Photobacterium symbiosis exemplifies this balance, as tropical siphonfish (Siphamia spp.) form a highly specific association with the bioluminescent bacterium Photobacterium mandapamensis, though it is unknown whether this specificity extends to temperate species of siphonfish. Here, we use long-read genome sequencing and functional assays to characterize the strain-level diversity of symbionts isolated from two temperate siphonfish hosts, Siphamia cephalotes and Siphamia roseigaster, and compare them to tropical isolates. We found that both hosts exclusively associate with P. mandapamensis in their light organs and that temperate strains form host-specific clades despite being collected in close proximity (< 5km). This is consistent with selective host filtering, microhabitat-driven adaptation, or conspecific host seeding. Pangenome analyses showed notable differences in accessory gene content, variation in the lux-rib operon, and a dramatic expansion of mobile genetic element (MGE) content in a subset of strains. We also identified the first host-derived P. mandapamensis isolate that is non-luminescent under laboratory conditions despite an intact lux-rib operon. Luminescence varied across strains, salinities, and temperature but was not correlated with the presence of luxF, with the majority of high-MGE strains exhibiting reduced light output. Together, these results extend the specificity of the Siphamia-Photobacterium symbiosis into temperate hosts and show that animals can maintain tight symbiont specificity despite the symbiont harboring substantial genomic and phenotypic flexibility at the strain level.